Living with the dead: when the body count rises, prey stick around

Abstract

Most terrestrial prey species are assumed to assess predation risk by detecting predators directly rather than using cues of previous attacks on conspecifics. However, such cues might represent valuable information, and prey can be expected to respond to the presence of congeners killed by enemies. Such cues are available in aphid colonies attacked by parasitic wasps because they do not remove parasitized hosts from the colony. Colonies are thus often a mixture of healthy, parasitized, and killed aphids, which corpses (mummies) stay attached to the plant and can be encountered by live aphids. Aphids exhibit a dispersal polyphenism. Recent studies show that they produce more winged offspring when directly exposed to natural enemies or to alarm pheromone emitted by conspecifics. We hypothesized that aphids perceive the corpses of congeners killed by parasitoids and respond by increasing the production of winged morphs, but we surprisingly found the opposite. We determined the adaptive value of this response by analyzing the foraging behavior of parasitoids in aphid colonies with killed aphids (mummies). Parasitoid females responded to the presence of mummies by reducing both their time allocation and parasitism activity in the patch. The strategy of aphids to reduce emigration (i.e., they produce more wingless morphs when mummies are present) is adaptive because the presence of killed congeners reduces parasitoid pressure on colonies. This demonstrates that the remains of individuals killed by natural enemies can still have an ecological relevance in prey populations and that enemy-induced phenotypic plasticity depends on the type of predation cues.